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Title of Thesis A Forest AnDark Evolutionary History of Norway Spruce Alexis R. Sullivan Department of Ecology and Environmental Science Umeå University 2020 This work is protected by the Swedish Copyright Legislation (Act 1960:729) Dissertation for PhD ISBN: 978-91-7855-211-5 Cover design by Thomas Ågren Electronic version available at: http://umu.diva-portal.org/ Printed by: CityPrint i Norr AB Umeå, Sweden 2020 Midway upon the journey of our life I found myself within a forest dark, for the straightforward path had been lost. How hard a thing it is to say what was this forest savage, rough, and stern, the very thought renews my fear. So bitter is it, death is little more; But to rehearse the good it also brought, I will speak of the other things I saw. Dante Alighieri, Inferno Translation modified from Henry Wadsworth Longfellow, with apologies List of Papers ......................................................................................................... iii Author Contributions ........................................................................................... iv Sammanfattning ..................................................................................................... v The big why? ........................................................................................................... 1 Gymnosperms: improbable model systems................................................... 2 Thesis aims and objectives ............................................................................... 5 Ecology and distribution ....................................................................................... 7 Genome structure and evolution ......................................................................... 9 Nuclei of dark matter ........................................................................................ 9 Are bigger genomes worse? ..................................................................... 13 Mitogenomes ................................................................................................... 14 Unique assembly challenges ..................................................................... 15 Mitogenome size variation....................................................................... 17 Plastomes .......................................................................................................... 19 Phylogenetics......................................................................................................... 23 The fossil history of spruce ............................................................................ 23 Phylogenetics: gene trees and species trees ................................................. 25 Hybridization ........................................................................................................ 30 Ubiquitous but cryptic? .................................................................................. 31 Promiscuous spruce ........................................................................................ 33 The rise of Norway spruce .................................................................................. 35 Climatic revolutions and the last trees standing ........................................ 35 Out of the ice. .............................................................................................. 39 … and into the fire: Spruce enters the Anthropocene ............................... 40 The future .............................................................................................................. 42 Acknowledgements .............................................................................................. 44 References .............................................................................................................. 46 i Abstract Embedded within the relationships among species is a dense forest of gene trees, each with a potentially unique and discordant history. Such widespread genealogical heterogeneity is expected, but embracing this hierarchy of discordance while reconstructing the histories of populations and species remains a major challenge. In this thesis, I studied the history of the genes and genomes contained within Norway spruce (Picea abies: Pinaceae), a forest tree distributed throughout boreal and montane Europe. I sequenced plastid genomes from all the commonly-recognized Picea species and developed a novel strategy to assemble the bacterial-sized mitochondrial genome of Norway spruce. Using multispecies coalescent network models, I reconstructed the relationships among populations of Norway spruce and the parapatric Siberian spruce (P. obovata) and distinguished between drift and hybridization as sources of phylogenetic discord. Norway spruce holds heterogenous histories at multiple levels of organization. Although organelle genomes are expected to be clonal and uniparentally inherited, the chloroplast genome held by Norway spruce originated after sexual recombination between two divergent lineages. In the mitochondrial genome, recombination creates a diverse population of genome arrangements subjected to drift and selection within individuals and populations. Genetic diversity among populations is shaped in nearly equal measure by divergence and hybridization. Norway spruce is discordance distilled. Key words: phylogenetics, genome assembly, recombination, Picea, hybridization, mitogenome, Norway spruce, phylogeography, phylogenetic networks, plastome ii List of Papers I. Sullivan, A.R., B. Schiffthaler, S.L. Thompson, N.R. Street, X.-R. Wang. 2017. Interspecific plastome recombination reflects ancient reticulate evolution in Picea (Pinaceae) Molecular Biology and Evolution 34:1689-1701. II. Sullivan, A.R., Y. Eldfjell, B. Schiffthaler, N. Delhomme, T. Asp, K.H. Hebelstrup, O. Keech, L. Öberg, I.A. Møller, L. Arvestad, N.R. Street, X-R. Wang. 2019. The mitogenome of Norway spruce and a reappraisal of mitochondrial recombination in plants. Genome Biology and Evolution 12: 3586–3598. III. Sullivan, A.R. J. Gao, Y. Jin, E. Mudrik, D. Politov, X-R. Wang. Evidence for the hybrid origin of Norway spruce. Manuscript. iii Author Contributions Paper I: ARS, SLT, and XRW conceived and designed the study. ARS and SLT collected samples. ARS performed all analyses with support from BS and NRS. ARS wrote the manuscript. ARS and XRW critically revised the manuscript with input from all authors. Paper II: ARS, IMM, NRS, LA, and XRW conceived and designed the study. BS, ND, and NRS obtained sequence data. TA, KHH, OK, LÖ, and IMM designed and implemented the ancient spruce sampling and sequencing. YE and LA designed and implemented the support vector machine. ND carried out the transcriptome assembly and annotation. ARS performed all other analyses with support from BS, ND, and NRS. ARS wrote the manuscript. ARS and XRW critically revised the manuscript with input from all authors. Paper III: ARS conceived and designed the study with advice from EM, DP, and XRW. EM and DP collected samples. JG and YJ performed laboratory experiments. ARS performed all analyses with support from XRW. ARS wrote the manuscript with input from XRW. All authors approved the manuscript. iv sammanfattning I kopplingarna mellan arter finns en tät skog av genfylogenier, där varje fylogeni kan uppvisa en historik som är unik och oenig med alla andra. Denna vidd av heterogen genealogi är förväntad, men att ta hänsyn till denna hierarki av disharmoni vid återskapandet av populationer och arters historik är fortsatt en enorm utmaning. I denna avhandling har jag studerat historiken hos gener och genom som återfinns hos gran (Picea abies: Pinaceae), ett skogsträd med en utbredning över boreala och bergiga delar av Europa. Jag sekvenserade plastidgenomen från de vedertagna Picea arterna och utvecklade en ny strategi för att pussla ihop det bakterie-stora mitokondriegenomet hos granen. Med hjälp av en sammanflätad multiart nätverks modell, kunde jag återskapa den evolutionära historiken hos gran och den parapatriska sibiriska granen (P. obovata) och särskilja genetisk drift och hybridisering som orsakerna bakom den fylogenetiska oenigheten. Granen har en heterogen historik på flera organisationsnivåer. Även om genomen hos organellerna förväntas nedärvas klonalt från endera föräldern, så har kloroplasten hos gran uppkommit från sexuell rekombination mellan två distinkta linjer. I mitokondriegenomet skapar rekombination en population av en mängd olika genomorganiseringar som erfar drift och urval på individ och populationsnivå. Granens populationer formas av en nästan lika del divergens som hybridisering. Gran är i det avseendet en koncentrerad form av disharmoni. v The big why? I began my PhD intending to study the effects of silviculture on the genetic diversity of Norway spruce (Picea abies: Pinaceae). As an immigrant to Sweden, I first consulted a couple of books to learn where, exactly, the species I signed up to study could be found. It did not take me long to discover that “Norway spruce” refers to a set of fuzzily defined and possibly polyphyletic groups. From there, I decided more fundamental questions needed to be addressed first: Do different groups of Norway spruce comprise a single species? What is the history of Norway spruce in an evolutionary context: where, when, and from whom did they evolve? Are spruce boundaries permeable, and if so, how much gene flow occurs? It also did not take me long to discover answering these questions would not be straightforward. My thesis results from my quest
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